Department of Biology, Tufts University, Medford, MA, 02155, USA.
ISME J. 2023 Sep;17(9):1504-1516. doi: 10.1038/s41396-023-01462-5. Epub 2023 Jul 31.
Experimental studies of microbial evolution have largely focused on monocultures of model organisms, but most microbes live in communities where interactions with other species may impact rates and modes of evolution. Using the cheese rind model microbial community, we determined how species interactions shape the evolution of the widespread food- and animal-associated bacterium Staphylococcus xylosus. We evolved S. xylosus for 450 generations alone or in co-culture with one of three microbes: the yeast Debaryomyces hansenii, the bacterium Brevibacterium aurantiacum, and the mold Penicillium solitum. We used the frequency of colony morphology mutants (pigment and colony texture phenotypes) and whole-genome sequencing of isolates to quantify phenotypic and genomic evolution. The yeast D. hansenii strongly promoted diversification of S. xylosus. By the end of the experiment, all populations co-cultured with the yeast were dominated by pigment and colony morphology mutant phenotypes. Populations of S. xylosus grown alone, with B. aurantiacum, or with P. solitum did not evolve novel phenotypic diversity. Whole-genome sequencing of individual mutant isolates across all four treatments identified numerous unique mutations in the operons for the SigB, Agr, and WalRK global regulators, but only in the D. hansenii treatment. Phenotyping and RNA-seq experiments highlighted altered pigment and biofilm production, spreading, stress tolerance, and metabolism of S. xylosus mutants. Fitness experiments revealed antagonistic pleiotropy, where beneficial mutations that evolved in the presence of the yeast had strong negative fitness effects in other biotic environments. This work demonstrates that bacterial-fungal interactions can have long-term evolutionary consequences within multispecies microbiomes by facilitating the evolution of strain diversity.
实验微生物进化研究主要集中在模式生物的单培养物上，但大多数微生物生活在与其他物种相互作用的群落中，这些相互作用可能会影响进化的速度和模式。使用奶酪皮模型微生物群落，我们确定了物种相互作用如何塑造广泛存在于食物和动物相关细菌——葡萄球菌（Staphylococcus xylosus）的进化。我们单独或与三种微生物中的一种共培养物进化了 450 代 S. xylosus：酵母汉逊德巴利酵母（Debaryomyces hansenii）、短杆菌（Brevibacterium aurantiacum）和青霉（Penicillium solitum）。我们使用菌落形态突变体（色素和菌落质地表型）的频率和分离株的全基因组测序来量化表型和基因组进化。酵母 D. hansenii 强烈促进了 S. xylosus 的多样化。在实验结束时，与酵母共培养的所有种群都以色素和菌落形态突变表型为主。单独生长的 S. xylosus、B. aurantiacum 或 P. solitum 的种群没有进化出新的表型多样性。对来自所有四种处理的单个突变体分离株的全基因组测序确定了 SigB、Agr 和 WalRK 全局调控因子操纵子中的许多独特突变，但仅在 D. hansenii 处理中。表型和 RNA-seq 实验突出了 S. xylosus 突变体的色素和生物膜产生、扩散、应激耐受和代谢的改变。适应性实验揭示了拮抗多效性，即在酵母存在下进化的有益突变在其他生物环境中具有强烈的负适应性影响。这项工作表明，细菌-真菌相互作用可以通过促进菌株多样性的进化，在多物种微生物组中产生长期的进化后果。
